Abstract:

We studied the amphibian community of the Parque Nacional da Serra dos Órgãos (PARNASO) for over thirty years. The area of 20,024 hectares has a steep altitudinal gradient (200-2,263 m a.s.l.), and it is located in the municipalities of Guapimirim, Magé, Petrópolis and Teresópolis, middle of the state of Rio de Janeiro, Brazil. Most data were obtained from sampling sites in the municipality of Teresópolis, with additional data from zoological collections and bibliography. We recorded 83 amphibian species distributed in two orders, Anura, 13 families: Aromobatidae (1), Brachycephalidae (11), Bufonidae (5), Centrolenidae (2), Craugastoridae (2), Cycloramphidae (8), Hemiphractidae (7), Hylidae (28), Hylodidae (6), Leptodactylidae (5), Microhylidae (1), Odontophrynidae (3), Phyllomedusidae (3) and Gymnophiona, one family: Siphonopidae (1). In addition, we present six species that occurs in the buffer zone. Ten of these species are endemic of the park, 18 have PARNASO as its type locality, and five the type locality is at the buffer zone.

Keywords:
Anura; biodiversity; conservation; disappeared species; endemic species; species richness

Resumo:

Estudamos a comunidade de anfíbios do Parque Nacional da Serra dos Órgãos (PARNASO) por mais de 30 anos. A área de 20.024 hectares possui um gradiente altitudinal de 200 a 2.263m acima do nível do mar, e está localizada nos municípios de Guapimirim, Magé, Petrópolis e Teresópolis, que ficam no meio do estado do Rio de Janeiro, Brasil. A maioria das coletas foram feitas no município de Teresópolis, com dados adicionais de outras coleções zoológicas e de bibliografia. Foram registradas ao todo 83 espécies de anfíbios distribuídos em duas ordens, Anura, 13 famílias: Aromobatidae (1), Brachycephalidae (11), Bufonidae (5), Centrolenidae (2), Craugastoridae (2), Cycloramphidae (8), Hemiphractidae (7), Hylidae (28), Hylodidae (6), Leptodactylidae (5), Microhylidae (1), Odontophrynidae (3), Phyllomedusidae (3) e Gymnophiona, uma família: Siphonopidae (1). Foram registradas, também, seis espécies que ocorrem na zona de amortecimento. Destas espécies 10 são endêmicas, 18 têm o PARNASO como localidade tipo e cinco têm a localidade tipo na zona de amortecimento.

Palavras-chave:
Anura; área montanhosa; biodiversidade; conservação; espécies desaparecidas; espécies endêmicas; inventário; Mata Atlântica; riqueza de espécies

Introduction

The Atlantic Rain Forest is a hotspot of biodiversity that harbors a large number of endemic species of vertebrates (Myers et al. 2000MYERS, N., MITTERMEYER, R.A., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.). More than 500 species of amphibians inhabit this biome, of which around 90% are endemic (Morellato & Haddad 2000MORELLATO, P. & HADDAD, C.F.B. 2000. Introduction: The Brazilian Atlantic Forest. Biotropica 32:786-792., Haddad et al. 2013HADDAD, C.F.B., TOLEDO, L.F., PRADO, C.P.A., LOEBMANN, D., GASPARINI, J.L. & SAZIMA, I. 2013. Anfíbios da Mata Atlântica: Diversidade e Biologia. Anolisbook, São Paulo, SP, Brazil.). The Atlantic Forest is one of the ecosystems mostly threatened by human activities around the world (Myers et al. 2000MYERS, N., MITTERMEYER, R.A., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.), and now it is reduced to a few fragments with only 12% of its original area (Ribeiro et al. 2009RIBEIRO, M.C., METZGER, J.P., MARTENSEN, A.C., PONZONI, F.J. & HIROTA, M.M. 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142:1141-1153.).

Located in the Atlantic Forest, the most devastated of Brazilian ecosystems, the Serra dos Órgãos National Park (Parque Nacional da Serra dos Órgãos - PARNASO) was created on November 30, 1939, being the third national park in the country. Initially covered an area of 10,653 hectares in the municipalities of Petrópolis, Guapimirim, Magé and Teresópolis, state of Rio de Janeiro (Cronemberger & Castro 2007CRONEMBERGER, C. & VIVEIROS DE CASTRO, E.B. 2007. Ciência e Conservação na Serra dos Órgãos. Ibama/Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, DF, Brazil.). In 2008, its area was expanded, and now comprises 20,024 hectares (ICMBIO 2008ICMBIO. 2008. Plano de manejo do Parque Nacional da Serra dos Órgãos. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, Brasil.). Nowadays, the Serra dos Órgãos National Park represents one of the few remaining spots of biodiversity in the state of Rio de Janeiro and stands out by protecting important water sources that feed two main watersheds, the Paraíba do Sul and Baía de Guanabara (Cronemberger & Castro 2007CRONEMBERGER, C. & VIVEIROS DE CASTRO, E.B. 2007. Ciência e Conservação na Serra dos Órgãos. Ibama/Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, DF, Brazil.).

PARNASO has altitudes ranging from 200 m to 2263 m above sea level (a.s.l.). The park climate is tropical super humid (80% to 90% relative humidity), with an annual average temperature ranging from 13° C to 23° C, except for the elevation areas higher than 800 m a.s.l., which reaches the maximum average annual temperature of 19º C and the minimum of -5° C during the winter. The average annual rainfall ranges from 1,500 mm to 3,000 mm, with higher concentrations of rain during the summer (December to March), and dry season in the winter (June to August; Cronemberger & Castro 2007CRONEMBERGER, C. & VIVEIROS DE CASTRO, E.B. 2007. Ciência e Conservação na Serra dos Órgãos. Ibama/Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, DF, Brazil.).

Amphibians are considered good indicators of environmental conditions due to its vulnerability to environmental changes (Wells 2007WELLS, K.D. 2007. The ecology and behavior of amphibians. University of Chicago Press, Chicago, IL, USA.). This characteristic associated with other factors such as amphibian’s habitats occupied by human activities, increased ultraviolet light, infectious diseases and climate changes have led amphibians’ populations to decline in the last decades (Stebbins & Cohen 1995STEBBINS, R.C. & COHEN, N.W. 1995. A Natural History of Amphibians. Princeton University Press, Princeton, NJ, USA., Gardner 2001GARDNER, T. 2001. Declining amphibians populations: a global phenomenon in conservation biology. Anim. Biodiv. Conserv. 24:25-44.). In this scenario, PARNASO is highlighted for being the type locality of several species, including some species endemic to the park (ICMBIO 2008ICMBIO. 2008. Plano de manejo do Parque Nacional da Serra dos Órgãos. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, Brasil.).

The main goal of this study is to present an updated checklist of the species occurring in the PARNASO area, encouraging researches on the species that lives there, as their taxonomy, behavior and natural history; and to help drive the management of the amphibian biodiversity in this conservation area.

Material and Methods

Our fieldwork at PARNASO began in 1962 by late Professor Eugenio Izecksohn, and we carried it until 2019, totaling 230 surveys during the rainy and dry seasons. During data collection, around three collectors worked at least three days. We performed two complementary methods for sampling the adults: active and auditory search (see Calleffo 2002CALLEFFO, M.E.V. 2002. Anfíbios. In Técnicas de coleta e preparação de vertebrados para fins científicos e didáticos (P. Auricchio & M.G. Salomão, eds.). Instituto Pau Brasil de História Natural, São Paulo, SP, Brasil, p 43-74.). For the capture of tadpoles, we used sieves (see Heyer et al. 1994HEYER, W.R., DONNELLY, M.A., MCDIARMID, R.W., HAYEK, L.C. & FOSTER, M. 1994. Measuring and monitoring biological diversity standard methods for amphibians. Smithsonian Institution Press, Washington, DC, USA.). Adults and tadpoles were collected, photographed, and then anesthetized and fixed according to the Brazilian law (CONCEA 2016CONCEA 2016. Diretriz Brasileira para o Cuidado e a Utilização de Animais em Atividades de Ensino ou de Pesquisa Científica. Available from https://www.mctic.gov.br/mctic/export/sites/institucional/institucional/concea/arquivos/legislacao/resolucoes_normativas/Resolucao-Normativa-CONCEA-n-30-de-02.02.2016-D.O.U.-de-03.02.2016-Secao-I-Pag.-03.pdf [Accessed 28 March 2020]
https://www.mctic.gov.br/mctic/export/si... ). Specimens were deposited at the amphibian collection of the Universidade Federal do Rio de Janeiro (ZUFRJ) and at the amphibian collection of Universidade Federal do Estado do Rio de Janeiro (UNIRIO). During this period, we obtained information on the natural history and distribution of the species from the park.

Additional data were obtained from the amphibian’s collections of the Eugênio Izecksohn (EI, Universidade Federal Rural do Rio de Janeiro), of Museu Nacional do Rio de Janeiro (MNRJ), of Kansas University (KU) and from bibliography (see Table 1). We also include a list of species that can be found in the buffer zone, including Represa dos Guinle and Granja Comary, in Teresópolis municipality.

These sources encompass more than 50 years of fieldwork in the area. Examined specimens are found in Appendix 3. Species richness estimates and Jackknife index (JK) were calculated using the software EstimateS 9.1.0 (Colwel 2013COLWELL, R.K. 2013. EstimateS 9.1.0. Statistical estimation of species richness and shared species form samples. Available at http://viceroy.eeb.uconn.edu/estimates.
http://viceroy.eeb.uconn.edu/estimates... ) with 1,000 randomizations. First order JK was chosen because it is indicated for possibly biased samples and performed best on both simulated and real datasets (Walther & Morand 1998WALTHER, B. A. & MORAND, S. 1998. Comparative performance of species richness estimation methods. Parasitology 116:395-405., Chao & Chiu, 2016CHAO, A. & CHIU, C. H. 2016. Nonparametric estimation and comparison of species richness. eLS, 1-11. https://doi.org/10.1002/9780470015902.a0026329
https://doi.org/10.1002/9780470015902.a0... ). The results were plotted in a graph, together with the species accumulation curve, on Microsoft Excel v. 1912. For these calculations, we excluded records that did not involve our team. Taxonomic nomenclature follows Frost (2020)FROST, D. (2020) Amphibian Species of the World: An Online Reference. Version 6.1. Available from http://research.amnh.org/herpetology/amphibia/index.html [Accessed 21 March 2020].
http://research.amnh.org/herpetology/amp... .

The sampling was more intense in places frequently visited by tourists, such as the swimming pool and dam, the trails Cartão Postal, Mozart Catão, Pedra do Sino, Primavera and Suspensa, all at the headquarters of Teresópolis; and the banks of Soberbo River, also in Teresópolis. We also sampled restricted places, just allowed to researchers, as the Rancho Frio trail, and more remote areas, such as the regions of Pedra do Sino at Teresópolis, Garrafão in Guapimirim, and Pico do Açu at Petrópolis (Figures 1 and 2).

Figure 1
Map of PARNASO showing the main sampling sites. Red line: limits of PARNASO. Orange line: main trail from Petrópolis to Teresópolis. Green star: trails in the Petrópolis headquarters. Green triangle: Pico do Açu (Açu peak). Green circle: “Pedra do Sino”. Blue triangle: trails in the Teresópolis headquarters. Blue circle: park administration and swimming pool. Blue star: trails in the Guapimirim headquarters.

Figure 2
Examples of sampled environments. (A) and (C) streams in primary forest. (B) artificial lake known as “swimming pool”. (D) secondary forest. (E) stream in secondary forest.

Results

We recorded 83 species (Table 1) within the park belonging to two orders and 14 families (Figure 3): order Anura, Arobomatidae (1 sp.); Brachycephalidae (11 spp.); Bufonidae (5 spp.); Centrolenidae (2 spp.); Craugastoridae (2 spp.); Cycloramphidae (8 spp.); Hemiphractidae (7 spp.); Hylidae (28 spp.); Hylodidae (6 spp.); Leptodactylidae (5 spp.); Microhylidae (1 sp.); Odontrophinidae (3 spp.); Phyllomedusidae (3 spp.); order Gymnophiona, Siphonopidae (1 spp.). Ten of these species are considered endemic of the park, 18 have PARNASO as its type locality, and five the type locality is at the buffer zone (Table 1). The species accumulation, species richness estimates and Jackknife index curves are presented in the Figure 4. The species accumulation curve shows a fast increase followed by a decreasing in the number of new species found, with a tendency of stabilization in its end, reaching 69 species. The superior limit of the confidence interval of the richness curve estimates 78 species within the park, while the Jackknife frequency estimates the presence of 88 species. Figures 5-7 illustrates some of the recorded species.

Figure 3
Species richness per family of the amphibians from PARNASO.

Figure 4
Sampling effort and species richness in PARNASO. Observed species accumulation curve, estimated species accumulation curve and estimated species richness. Estimated species accumulation curve calculated through Jackknife index using 1000 replications. Estimated species richness based in 1000 randomizations, including 95% confidence interval (CI). The years with no sampling were removed.

Figure 5
Species of anurans recorded on PARNASO. (A) Fritziana Izecksohni. (B) Fritziana cf. fissilis. (C) Fritziana ohausi. (D) Fritziana goeldii. (E) Gastrotheca albolineata. (F) Gatrotheca ernestoi. (G) Gastrotheca fulvorufa. (H) Cycloramphus eleutherodactylus. (I) Cycloramphus organensis. (J) Cycloramphus stejnegeri, fixed specimen. (K) Thoropa petropolitana, fixed specimen. (L) Dendrophryniscus organensis.

Figure 6
Species of anurans recorded on PARNASO. (A) Brachycephalus ephippium. (B) Ischnocnema erythromera. (C) Haddadus binotatus. (D) Aplastodiscus arildae. (E) Aplastodiscus eugenioi. (F) Aplastodiscus flumineus. (G) Aplastodiscus leucopygius. (H) Aplastodiscus musicus. (I) Bokermannohyla carvalhoi. (J) Bokermannohyla circumdata. (K) Hylodes pipilans. (L) Megaelosia goeldii.

Figure 7
Species of anurans recorded on PARNASO. (A) Ololygon albicans. (B) Ololygon flavoguttata. (C) Ololygon hiemalis, fixed specimen. (D) Ololygon melloi. (E) Ololygon v-signata. (F) Scinax hayii. (G) Adenomera marmorata. (H) Myersiella microps. (I) Proceratophrys appendiculata.

Other six species were recorded at the buffer zone (Table 2), belonging to two orders and four families: order Anura, Ceratophryidae (1 sp.); Hylidae (1 sp.); Leptodactylidae (2 spp.); and order Gymnophiona, Siphonopidae (2 sp.).

Examined material is listed on Appendix 1.

Discussion

Considering the more than 1,000 described species of Brazilian amphibians, the amphibian fauna of PARNASO together with its buffer zone, represent almost 10% of all country diversity, highlighting the importance of the park in the preservation of this group.

Previously, two other inventories were conducted in the area. Campos & Lourenço-de-Moraes (2017)CAMPOS, F.S. & LOURENÇO-DE-MORAES, R. 2017. Anurans from the mountain chain Serra do Mar: a critical area for amphibian conservation in the Atlantic Forest, Brazil. Herpetol. Notes 10:547-560. http://www.biotaxa.org/hn/article/view/31357
http://www.biotaxa.org/hn/article/view/3... reported 25 species, of which Dendropsophus giesleri (Mertens, 1950) and Physalaemus cuvieri Fitzinger, 1826 were not found in the present study. The authors did not mention the voucher specimens; thus, we could not verify the species identification. The second inventory was conducted by Folly et al. (2016)FOLLY, M., BEZERRA, A.M., RUGGERI, J., HEPP, F., CARVALHO-E-SILVA, A.M.P.T. , GOMES, M.R. & CARVALHO-E-SILVA, S.P. 2016. Anuran fauna of the high-elevation areas of the Parque Nacional da Serra dos Órgãos (PARNASO), southeastern Brazil. Oecol. Aust. 20:247-258. http://dx.doi.org/10.4257/oeco.2016.2002.08
http://dx.doi.org/10.4257/oeco.2016.2002... focusing on the anuran species restricted to the high elevation areas of PARNASO, recording 28 species, all included in the present study.

According to Dorigo et al. (2018)DORIGO, T.A., VRCIBRADIC, D. & ROCHA, C.F.D. 2018. The amphibians of the state of Rio de Janeiro, Brazil: an updated and commented list. Pap. Avulsos Zool. 58:1-11. http://doi.org/10.11606/1807-0205/2018.58.05
http://doi.org/10.11606/1807-0205/2018.5... , the state of Rio de Janeiro has 201 species distributed in 51 genera and 16 families of amphibians, of which 54 are considered endemic. After that, three more species were described, all endemic to the state: Fritziana izecksohni Folly, Hepp & Carvalho-e-Silva, 2018FOLLY, M., HEPP, F. & CARVALHO-E-SILVA, S.P. 2018. A new bromeligenous species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from high elevations in the Serra Dos Órgãos, Rio de Janeiro, Brazil. Herpetologica 74:58-72. https://doi.org/10.1655/Herpetologica-D-16-00035
https://doi.org/10.1655/Herpetologica-D-... , Ischnocnema parnaso Taucce, Canedo, Parreiras, Drummond, Nogueira-Costa, & Haddad, 2018TAUCCE, P.P.G., CANEDO, C. & HADDAD, C.F.B. 2018a. Two new species of Ischnocnema (Anura: Brachycephalidae) from southeastern Brazil and their phylogenetic position within the I. guentheri series. Herpetol. Monogr. 32:1-21., and Phasmahyla lisbella Pereira, Rocha, Folly, Silva, & Santana, 2018PEREIRA, E.A., ROCHA, L.C.L., FOLLY, H., SILVA, H.R. & SANTANA, D.J. 2018. A new species of spotted leaf frog, genus Phasmahyla (Amphibia, Phyllomedusidae) from Southeast Brazil. PeerJ 6:1-22. https://doi.org/10.7717/peerj.4900
https://doi.org/10.7717/peerj.4900... (Folly et al. 2018FOLLY, M., HEPP, F. & CARVALHO-E-SILVA, S.P. 2018. A new bromeligenous species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from high elevations in the Serra Dos Órgãos, Rio de Janeiro, Brazil. Herpetologica 74:58-72. https://doi.org/10.1655/Herpetologica-D-16-00035
https://doi.org/10.1655/Herpetologica-D-... , Taucce et al. 2018bTAUCCE, P.P.G., CANEDO, C., PARREIRAS, J.S., DRUMMOND, L.O., NOGUEIRA-COSTA, P. & HADDAD, C.F.B. 2018b. Molecular phylogeny of Ischnocnema (Anura: Brachycephalidae) with the redefinition of its series and the description of two new species. Mol Phylogenet Evol 128:123-146. https://doi.org/10.1016/j.ympev.2018.06.042
https://doi.org/10.1016/j.ympev.2018.06.... , Pereira et al. 2018PEREIRA, E.A., ROCHA, L.C.L., FOLLY, H., SILVA, H.R. & SANTANA, D.J. 2018. A new species of spotted leaf frog, genus Phasmahyla (Amphibia, Phyllomedusidae) from Southeast Brazil. PeerJ 6:1-22. https://doi.org/10.7717/peerj.4900
https://doi.org/10.7717/peerj.4900... , respectively). Whereas endemic species are more prone to extinction (Isik 2010ISIK, K. 2010. Rare and endemic species: Why are they prone to extinction? Turk. J. Bot. 35:411-417.), the park plays a major role protecting 10 species, around 3% of the Rio de Janeiro state biodiversity, that only occurs over there.

The amphibian diversity found in this study places the PARNASO as the natural reserve with highest species richness in the Atlantic Forest area, surpassing the Paranapiacaba Biological Reserve, in the state of São Paulo, considered as the greatest one by Verdade et al. (2009)VERDADE, V.K., RODRIGUES, M.T. & PAVAN, D. 2009. Anfíbios Anuros da região da Estação Biológica do Alto da Serra de Paranapiacaba. Pp. 579-604. In: Patrimônio da Reserva Biológica do Alto da Serra de Paranapiacaba. A antiga Estação Biológica do Alto da Serra. Lopes, M.I.M.S., M. Kirizawa, and M.R.F. Melo (Eds.). Secretaria do Meio Ambiente do Estado de São Paulo, São Paulo, SP, Brazil. with 69 species at that time, and Serra Bonita, in the state of Bahia, considered a new hotspot in Brazil, with 80 species (Dias et al. 2014DIAS, I.R., MEDEIROS, T.T., NOVA, M.F.V. & SOLÉ, M. 2014. Amphibians of Serra Bonita, southern Bahia: a new hotpoint within Brazil’s Atlantic Forest hotspot. ZooKeys 449:105-130. https://doi.org/10.3897/zookeys.449.7494
https://doi.org/10.3897/zookeys.449.7494... ). On a national scale, species inventories are not available for several natural reserves individually. As long as we could track, no individual strict protection reserve area in Brazil surpasses the PARNASO in number of amphibian species. Even the largest tropical forest reserves in the world located in Brazil (according to UNEP-WCMC and IUCN. 2018IUCN. 2018. World Database on Protected Areas. Available from www.protectedplanet.net [Accessed 10 July 2018]
www.protectedplanet.net... ) that have amphibian’s species inventories published have lower richness: Estação Ecológica Grão-Pará (42,000 km², 70 species; Avila-Pires et al. 2010AVILA-PIRES, T.C.S., HOOGMOED, M.S. & ROCHA, W.A. 2010. Notes on Vertebrates of Northern Pará, Brazil: a forgotten part of the Guianan Region, I. Herpetofauna. Bol. Mus. Para. Emilio Goeldi. Sér. Ciênc. Nat. 5:13-112.) and Parque Nacional Montanhas do Tumucumaque (38,600 km², 70 species; Lima 2008LIMA, J.D. 2008. A herpetofauna do Parque Nacional das Montanhas do Tumucumaque, Amapá, Brasil, Expedições I a V. In Inventários Biológicos Rápidos no Parque Nacional Montanhas do Tumucumaque, Amapá, Brasil (E. Bernard, ed.). RAP Bulletin of Biological Assessment, Arlington, VA, USA, p 38-50.), both in the state of Pará, Brazil, on Amazonia area.

The number of amphibian species of PARNASO has increased in the last years, either by new records (e.g., Ololygon hiemalis, Caram et al. 2011CARAM, J., LUNA-DIAS, C., GOMES, M.R. & CARVALHO-E-SILVA, S.P. 2011. Distribution extension of Scinax hiemalis (Haddad & Pombal, 1987) and new state record from Rio de Janeiro, southeastern Brazil (Anura: Amphibia: Hylidae). Herpetol. Notes 4:153-154., Rhinella crucifer, Marques et al. 2006MARQUES, R.A., ANNUNZIATTA, B.B. & CARVALHO-E-SILVA, A.M.P.T. 2006. Bufo crucifer. Brazil. Rio de Janeiro - Geographic Distribution. Herpetol. Rev. 37:98-99.) or by the discovery of new species (e.g., Ischnocnema parnaso, Tauce et al. 2018bTAUCCE, P.P.G., CANEDO, C., PARREIRAS, J.S., DRUMMOND, L.O., NOGUEIRA-COSTA, P. & HADDAD, C.F.B. 2018b. Molecular phylogeny of Ischnocnema (Anura: Brachycephalidae) with the redefinition of its series and the description of two new species. Mol Phylogenet Evol 128:123-146. https://doi.org/10.1016/j.ympev.2018.06.042
https://doi.org/10.1016/j.ympev.2018.06.... , Fritziana izecksohni, Folly et al. 2018FOLLY, M., HEPP, F. & CARVALHO-E-SILVA, S.P. 2018. A new bromeligenous species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from high elevations in the Serra Dos Órgãos, Rio de Janeiro, Brazil. Herpetologica 74:58-72. https://doi.org/10.1655/Herpetologica-D-16-00035
https://doi.org/10.1655/Herpetologica-D-... , Dendrophryniscus organensis Carvalho-e-Silva et al., 2013, Cycloramphus organensis Weber et al., 2011WEBER, L.N., VERDADE, V.K., SALLES, R.O.L., FOUQUET, A. & CARVALHO-E-SILVA, S.P. 2011. A new species of Cycloramphus Tschudi (Anura: Cycloramphidae) from the Parque Nacional da Serra dos Órgãos, southeastern Brazil. Zootaxa 2737:19-33., Hylodes pipilans Canedo & Pombal, 2007, Aplastodiscus eugenioi Carvalho-e-Silva & Carvalho-e-Silva, 2005, Ololygon melloi Peixoto, 1989PEIXOTO, O.L. 1989. Duas novas espécies de Ololygon do grupo perpusilla (Amphibia, Anura, Hylidae). Arq. Univ. Fed. Rur. Rio de J. 11:27-37., Bokermannohyla carvalhoi Peixoto, 1981). During the last few years, members of our team participated in the descriptions of five of these endemic species (Peixoto 1989PEIXOTO, O.L. 1989. Duas novas espécies de Ololygon do grupo perpusilla (Amphibia, Anura, Hylidae). Arq. Univ. Fed. Rur. Rio de J. 11:27-37., Weber et al. 2011WEBER, L.N., VERDADE, V.K., SALLES, R.O.L., FOUQUET, A. & CARVALHO-E-SILVA, S.P. 2011. A new species of Cycloramphus Tschudi (Anura: Cycloramphidae) from the Parque Nacional da Serra dos Órgãos, southeastern Brazil. Zootaxa 2737:19-33., Carvalho-e-Silva et al. 2013, Folly et al. 2018FOLLY, M., HEPP, F. & CARVALHO-E-SILVA, S.P. 2018. A new bromeligenous species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from high elevations in the Serra Dos Órgãos, Rio de Janeiro, Brazil. Herpetologica 74:58-72. https://doi.org/10.1655/Herpetologica-D-16-00035
https://doi.org/10.1655/Herpetologica-D-... ) (Table 1).

According to the Red List of the International Union for Conservation of Nature and Natural Resources (IUCN 2019INTERNATIONAL UNION FOR THE CONSERVATION OF NATURE (IUCN). 2019. IUCN Red List of Threatened Species. http://www.iucnredlist.org. [Accessed 21 March 2020].
http://www.iucnredlist.org... ), 57 of the registered species are classified as Least Concern (LC), 20 have not enough information on its conservation (DD), two are classified as Near Threatened (NT), two are classified as Vulnerable (VU) and two have unknown data (see Table 1). Still, in the Brazilian list of endangered species (ICMBio 2016ICMBIO. 2016. Sumário Executivo do Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, Brasil.), three species are listed: one Vulnerable (Allobates olfersioides) and two Endangered (Cycloramphus ohausi and Thoropa petropolitana).

Despite our data do not allow abundance analysis, some of the species as Aplastodiscus arildae, Brachycephalus ephippium, Ischnocnema parva, Ololygon albicans and Scinax hayii, were found in most of our surveys, indicating that they are probably abundant inside the Park.

Some species have become rare or even disappeared from PARNASO without an apparent reason, such as Aplastodiscus musicus, disappeared for more than 20 years and reencountered in 2016 (Bezerra et al. 2020BEZERRA, A.M. PASSOS, L.O., DE LUNA-DIAS, C., QUINTANILHA, A.S. & CARVALHO-E-SILVA, S.P. 2020. A Missing Piece of the Puzzle: Re-encounter of Aplastodiscus musicus, Its Call, and Phylogenetic Placement (Anura: Hylidae: Cophomantini). Herpetologica 76:74-82. https://doi.org/10.1655/Herpetologica-D-18-00061
https://doi.org/10.1655/Herpetologica-D-... ); Allobates olfersioides, which has not been found since 1969 in the park, and has been reported as declining or disappeared from other localities (Weygoldt 1989WEYGOLDT, P. 1989. Changes in the composition of mountain stream frog communities in the Atlantic mountains of Brazil: frogs as indicators of environmental deterioration? Stud. Neotrop. Fauna Environ. 24:249-255. http://dx.doi.org/10.1080/01650528909360795
http://dx.doi.org/10.1080/01650528909360... , Izecksohn & Carvalho-e-Silva 2001IZECKSOHN E. & CARVALHO-E-SILVA, S.P. 2001. Anfíbios do município do Rio de Janeiro. Editora UFRJ, Rio de Janeiro, RJ., Gasparini et al. 2007GASPARINI, J.L., ALMEIDA, A.P., CRUZ, C.A.G. & FEIO, R.N. 2007. Os anfíbios ameaçados de extinção no Estado do Espírito Santo. In Espécies da fauna ameaçadas de extinção no Estado do Espírito Santo (M. Passamani & S.L. Mendes, eds). Instituto de Pesquisas da Mata Atlântica (IPEMA), Vitória, ES, Brazil., p.75-86., Caram et al. 2016CARAM, J. , GOMES, M.R. , LUNA-DIAS, C. & CARVALHO-E-SILVA, S.P. 2016. Updated list of anurans from Floresta Nacional Mário Xavier, Seropédica, Rio de Janeiro, Brazil: changes from 1990 to 2012. Check List 12:1-7. http://dx.doi.org/10.15560/12.6.1997
http://dx.doi.org/10.15560/12.6.1997... ); and Vitreorana uranoscopa, which also disappeared for almost 20 years, and was reencountered by us in 2009. Similar disappearance was reported by Izecksohn & Carvalho-e-Silva (2001)IUCN. 2018. World Database on Protected Areas. Available from www.protectedplanet.net [Accessed 10 July 2018]
www.protectedplanet.net... for the Parque Nacional da Floresta da Tijuca, municipality of Rio de Janeiro, where the species was also found recently (AMPTCS and SPCS pers. obs.).

Only one individual of Proceratophrys melanopogon was recorded in PARNASO. As noted by Izecksohn et al. (1998)IZECKSOHN E., CRUZ, C.A.G. & PEIXOTO, O.L. 1998. Sobre Proceratophrys appendiculata e algumas espécies afins (Amphibia: Anura: Leptodactylidae). Rev. Univ. Rural, Sér. Ciênc. Vida 20:37-54., this individual was collected in 1952, together with five individuals of P. appendiculata, a common species within the park boundaries. Although common in the locality of Macaé de Cima (Izecksohn et al. 1998IZECKSOHN E., CRUZ, C.A.G. & PEIXOTO, O.L. 1998. Sobre Proceratophrys appendiculata e algumas espécies afins (Amphibia: Anura: Leptodactylidae). Rev. Univ. Rural, Sér. Ciênc. Vida 20:37-54., Prado & Pombal Jr. 2008PRADO, G.M. & POMBAL, J.P. Jr. 2008. Espécies de Proceratophrys Miranda-Ribeiro, 1920 com apêndices palpebrais (Anura: Cycloramphidae). Arq. Zool. 39:1-85. http://dx.doi.org/10.11606/issn.2176-7793.v39i1p1-85
http://dx.doi.org/10.11606/issn.2176-779... ), approximately 50 km east from PARNASO, P. melanopogon remains with only one register in PARNASO and its vicinity.

Gehara et al. (2013)GEHARA, M., CANEDO, C., HADDAD, C.F.B & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14:973-982. https://doi.org/10.1007/s10592-013-0488-5
https://doi.org/10.1007/s10592-013-0488-... restricted the name Ischnocnema guentheri to just one population of the city of Rio de Janeiro, Brazil. Other populations formerly associated with this name from the states of Santa Catarina, Paraná, São Paulo, Minas Gerais, and other populations from the state of Rio de Janeiro, actually represent unnamed species. Due to that, we could not determine the specific status of Ischnocnema aff. guentheri. Despite recent taxonomic efforts (e.g., Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14:973-982. https://doi.org/10.1007/s10592-013-0488-5
https://doi.org/10.1007/s10592-013-0488-... , Taucce et al. 2018aTAUCCE, P.P.G., CANEDO, C. & HADDAD, C.F.B. 2018a. Two new species of Ischnocnema (Anura: Brachycephalidae) from southeastern Brazil and their phylogenetic position within the I. guentheri series. Herpetol. Monogr. 32:1-21., bTAUCCE, P.P.G., CANEDO, C., PARREIRAS, J.S., DRUMMOND, L.O., NOGUEIRA-COSTA, P. & HADDAD, C.F.B. 2018b. Molecular phylogeny of Ischnocnema (Anura: Brachycephalidae) with the redefinition of its series and the description of two new species. Mol Phylogenet Evol 128:123-146. https://doi.org/10.1016/j.ympev.2018.06.042
https://doi.org/10.1016/j.ympev.2018.06.... ), the Ischnocnema guentheri species series is still being taxonomically confusing, composed by several morphologically cryptic species (Taucce et al. 2018aTAUCCE, P.P.G., CANEDO, C. & HADDAD, C.F.B. 2018a. Two new species of Ischnocnema (Anura: Brachycephalidae) from southeastern Brazil and their phylogenetic position within the I. guentheri series. Herpetol. Monogr. 32:1-21.). New efforts must be done to clarify this question, specially involving molecular and acoustic data, which have shown great relevance to the taxonomy of this species series (e.g., Kwet & Solé 2005KWET, A. & SOLÉ, M. 2005. Validation of Hylodes henselii Peters, 1870, from Southern Brazil and description of acoustic variation in Eleutherodactylus guentheri (Anura: Leptodactylidae). J. Herpetol. 39:521-532. https://www.jstor.org/stable/4092841
https://www.jstor.org/stable/4092841... , Gehara et al. 2013GEHARA, M., CANEDO, C., HADDAD, C.F.B & VENCES, M. 2013. From widespread to microendemic: molecular and acoustic analyses show that Ischnocnema guentheri (Amphibia: Brachycephalidae) is endemic to Rio de Janeiro, Brazil. Conserv. Genet. 14:973-982. https://doi.org/10.1007/s10592-013-0488-5
https://doi.org/10.1007/s10592-013-0488-... , Hepp & Canedo 2013HEPP, F. & CANEDO, C. 2013. Advertisement and aggressive calls of Ischnocnema oea (Heyer, 1984) (Anura, Brachycephalidae). Zootaxa 3710:197-199. http://dx.doi.org/10.11646/zootaxa.3710.2.6
http://dx.doi.org/10.11646/zootaxa.3710.... , Taucce et al. 2018aTAUCCE, P.P.G., CANEDO, C. & HADDAD, C.F.B. 2018a. Two new species of Ischnocnema (Anura: Brachycephalidae) from southeastern Brazil and their phylogenetic position within the I. guentheri series. Herpetol. Monogr. 32:1-21., bTAUCCE, P.P.G., CANEDO, C., PARREIRAS, J.S., DRUMMOND, L.O., NOGUEIRA-COSTA, P. & HADDAD, C.F.B. 2018b. Molecular phylogeny of Ischnocnema (Anura: Brachycephalidae) with the redefinition of its series and the description of two new species. Mol Phylogenet Evol 128:123-146. https://doi.org/10.1016/j.ympev.2018.06.042
https://doi.org/10.1016/j.ympev.2018.06.... ).

The species accumulation curve represents the rate at which new species were recorded considering our continued sampling effort (Figure 4). The stabilization found at the end suggests that our sampling effort possibly recorded a number of species close to the real species richness occurring in PARNASO. The fast increase in the species accumulation curve followed by a decreasing in the number of new species recorded along the years is expected since the common and abundant species are usually found more easily, i.e. in the first expeditions, and along the years rare species are slowly being added (Ugland et al. 2003UGLAND, K.I., JOHN, S.G. & ELLINGSEN, K.E. 2003. The Species - Accumulation curve and estimation of species richness. J. Anim. Ecol. 72:888-897.). The superior limit of the confidence interval of the richness curve and the Jackknife frequency estimated a number of species close to the number that we recorded considering the additional data from literature and other collections.

Considering our effort time of more than 50 years, and more than 200 expeditions, it is expected the number of recorded species to be close to the real species richness occurring in PARNASO, as suggested by the stabilization at the final portion of the curve. Nevertheless, we would like to emphasize the importance of continue studying the PARNASO amphibian fauna, including taxonomic revisions, acoustic descriptions, population dynamics and every possible aspect of these taxa natural history. These studies are essential to aggregate knowledge about the species, a very important aspect of our basic science, which is the basis of all applied knowledge. These studies are also indispensable for the elaboration of management plans of PARNASO, maintaining these species preserved and in balance with their habitat.

Since its foundation, PARNASO was the scene for several studies on different topics involving amphibians, such as tadpole morphology and development (e.g., Carvalho-e-Silva & Carvalho-e-Silva 1994CARVALHO-E-SILVA, S.P. & CARVALHO-E-SILVA, A.M.P.T. 1994. Descrição das larvas de Ololygon albicans e de O. trapicheiroi com considerações sobre sua biologia (Amphibia, Anura, Hylidae). Braz. J. Biol. 54:55-62., Dias et al. 2013aDIAS P.H.S., CARVALHO-E-SILVA, A.M.P.T. & CARVALHO-E-SILVA, S.P. 2013a. Larval chondrocranium morphology of five species of Proceratophrys Miranda-Ribeiro (Amphibia; Anura; Odontophrynidae). Zootaxa 3683:427-438. http://dx.doi.org/10.11646/zootaxa.3683.4.6
http://dx.doi.org/10.11646/zootaxa.3683.... , Mongin & Carvalho-e-Silva 2013MONGIN, M.M. & CARVALHO-E-SILVA, A.M.P.T. 2013. Descrição da morfologia oral interna, ontogenia e redescrição do girino de Bokermannohyla circumdata (Cope, 1870) (Amphibia: Anura: Hylidae). Bol. Mus. Para. Emilio Goeldi. Sér. Ciênc. Nat. 8: 133-152., Silva et al. 2018SILVA, D.N., ROSA, F.C.B. & CARVALHO-E-SILVA, A.M.P.T. 2018. Ontogeny and Behavioral Aspects of the Tadpoles of Megaelosia goeldii (Baumann, 1912) (Amphibia, Anura, Hylodidae). Herpetol. Notes 11:629-639.), bioacoustics and breeding biology (e.g., Orrico et al. 2006ORRICO, V.G.D., CARVALHO-E-SILVA, A.M.P.T. & CARVALHO-E-SILVA, S.P. 2006. Redescription of the advertisement call of Aplastodiscus arildae (Cruz & Peixoto) and description of the call of Aplastodiscus weygoldti (Cruz & Peixoto) with general notes about the genus in Southeastern Brazil (Anura, Hylidae). Rev. Bras. Zool. 23:994-1001. http://dx.doi.org/10.1590/S0101-81752006000400003
http://dx.doi.org/10.1590/S0101-81752006... , Dias et al. 2013bDIAS, P.H.S., HEPP, F. & CARVALHO-E-SILVA, A.M.P.T. 2013b. Breeding biology and advertisement call of the horned leaf-frog, Proceratophrys appendiculata (Amphibia: Anura: Odontophrynidae). Zoologia 30:388-396. http://dx.doi.org/10.1590/S1984-46702013000400004
http://dx.doi.org/10.1590/S1984-46702013... ), histology (e.g., Felsemburgh & Gitirana 2008FELSEMBURGH, F.A. & GITIRANA, L.B. 2008. Avaliação morfológica do tegumento de fêmeas de Proceratophrys boiei. Espac. geogr. 11:59-72., Silva et al. 2017SILVA, H.A.M.D., SILVA-SOARES, T. & BRITO-GITIRANA, L. 2017. Comparative analysis of the integument of different tree frog species from Ololygon and Scinax genera (Anura: Hylidae). Zoologia 34:1-17. http://dx.doi.org/10.3897/zoologia.34.e20176
http://dx.doi.org/10.3897/zoologia.34.e2... ), osteology (e.g., Izecksohn et al. 2005IZECKSOHN E. , CARVALHO-E-SILVA, S.P. & FARIAS, I.D. 2005. Osteocrânio de Proceratophrys boiei, P. appendiculata e P. laticeps (Anura, Leptodactylidae). Rev. Bras. Zool. 22:225-229. http://dx.doi.org/10.1590/S0101-81752005000100028
http://dx.doi.org/10.1590/S0101-81752005... ), diet (e.g., Sabagh & Carvalho-e-Silva 2008SABAGH, L. & CARVALHO-E-SILVA, A.M.P.T. 2008. Feeding overlap in two sympatric species of Rhinella (Anura: Bufonidae) of the Atlantic Rain Forest. Rev. Bras. Zool. 25:247-253.), fungal infection or abnormalities (e.g., Dias & Carvalho-e-Silva 2012DIAS, P.H.S. & CARVALHO-E-SILVA, A.M.P.T. 2012. Records of abnormalities in Proceratophrys appendiculata (Günther, 1873) (Anura; Cycloramphidae; Alsodinae). Herpet. Notes 5:197-199., Ruggeri et al. 2017RUGGERI J., TOLEDO, L.F. & CARVALHO-E-SILVA, S.P. 2017. Stream tadpoles present high prevalence but low infection loads of Batrachochytrium dendrobatidis (Chytridiomycota). Hydrobiologia 806:303-311. https://doi.org/10.1007/s10750-017-3367-0
https://doi.org/10.1007/s10750-017-3367-... , Ruggeri et al. 2018RUGGERI, J., CARVALHO-E-SILVA, S.P., JAMES, T.Y. & TOLEDO, L.F. 2018. Amphibian chytrid infection is influenced by rainfall seasonality and water availability. Dis. Aquat. Organ. 127:107-115. https://doi.org/10.3354/dao03191
https://doi.org/10.3354/dao03191... ), besides dozens of academic works of undergraduate and PhD students. This highlights the importance of nature reserves, and of the PARNASO itself, not only for biodiversity conservation, but also to facilitate advances on its understanding and execution of fieldworks, generating essential knowledge to conservation decisions, and for the formation of new scientists.

Acknowledgments

We thank PARNASO staff, and all students who helped during these 50 years of field work. We also thank Fabio Hepp for the contribution throughout the confection of the manuscript. This study was supported by Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (grants #E-26/112.137/2008 and #E-26/111.638/2012) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; grants #312606/2017-6 and #311156/2013-4). We also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES/CNPq for the fellowships received. We are also grateful to Denise Rossa-Feres and another referee for suggestions int the text.

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